Saccades, salience and attention: the role of the lateral intraparietal area in visual behavior.

1Mahoney Center for Brain and Behavior, Center for Neurobiology and Behavior, Columbia University College of Physicians and Surgeons, and the New York State Psychiatric Institute, New York, NY 10032, USA. meg2008@columbia.edu

Abstract

Neural activity in the lateral intraparietal area (LIP) has been associated with attention to a location in visual space, and with the intention to make saccadic eye movement. In this study we show that neurons in LIP respond to recently flashed task-irrelevant stimuli and saccade targets brought into the receptive field by a saccade, although they respond much to the same stimuli when they are stable in the environment. LIP neurons respond to the appearance of a flashed distractor even when a monkey is planning a memory-guided delayed saccade elsewhere. We then show that a monkey's attention, as defined by an increase in contrast sensitivity, is pinned to the goal of a memory-guided saccade throughout the delay period, unless a distractor appears, in which case attention transiently moves to the site of the distractor and then returns to the goal of the saccade. LIP neurons respond to both the saccade goal and the distractor, and this activity correlates with the monkey's locus of attention. In particular, the activity of LIP neurons predicts when attention migrates from the distractor back to the saccade goal. We suggest that the activity in LIP provides a salience map that is interpreted by the oculomotor system as a saccade goal when a saccade is appropriate, and simultaneously is used by the visual system to determine the locus of attention.

Stable array task. An array of symbols remains on the screen unchanging throughout the task. (A) The monkey looks at a fixation point (black dot, marked FP) situated so no member of the array is in the receptive field (parabolic solid line, RF) of the neuron. (B) The fixation point jumps and monkey makes a saccade (arrow) to follow it, bringing the receptive field onto the spatial location of a symbol (in this case the X). Adapted from .

Activity of a neuron in LIP to a stimulus brought into its receptive field by different strategies. (A) The stimulus flashes in the receptive field during a fixation task. Raster diagrams, spike density plot (σ = 10 ms), and eye position (V: vertical, H: horizontal) are shown. Raster and spike density plots synchronized on the stimulus appearance. (B) Stable stimulus brought into receptive field by a saccade. Data synchronized on saccade onset. (C) Recently flashed stimulus brought into receptive field by the saccade. Data synchronized on saccade onset. Adapted from .

Stable target task. First panel: the monkey fixates so that all symbols in the array are outside the receptive field. Second panel: a cue appears, also outside the receptive field. Third panel: the fixation point jumps and the monkey makes a saccade that brings a symbol into the receptive field. In this example, the symbol in the receptive field matches the cue. Fourth panel: the fixation point disappears and the monkey makes a saccade to the symbol that matched the cue. Adapted from .

Activity of LIP neuron in the stable target task. Each subfigure consists of two panels. The cartoon above each panel shows the saccade upon which the underlying raster and spike density figures are synchronized on the saccade beginning. The first saccade brings a stable stimulus into the receptive field; the second saccade is made to the member of the stable array that matched the cue. (A) The monkey makes the second saccade to the receptive field. (B) The monkey makes the second saccade away from the receptive field. Adapted from .

Activity of LIP neuron in the black hole task. (A) Activity of a neuron in the stable target task. Left panel: activity synchronized on the appearance of the cue. Rasters, spike densities, horizontal (H) and vertical (V) eye position traces are shown. The heavy black line denotes the presence of the cue. Note that the cue is outside the receptive field of the neuron, and the activity develops slowly. Right panel: activity synchronized on the saccade beginning. (B) Activity of the same cell in the black hole task. Adapted from .

Memory-guided saccade and distractor tasks. (A) Memory-guided saccade. The monkey fixates the fixation point (FP), and a stimulus (the target) appears and disappears in the receptive field of the neuron. The monkey maintains fixation until the fixation point disappears, at which point the monkey makes a saccade to the remembered location of the vanished target. (B) Distractor task. The monkey fixates, the target appears in the receptive field, and in the interval 300–100 ms before the disappearance of the fixation point a task-irrelevant distractor appears in the receptive field. When the fixation point disappears, the monkey makes a saccade to the spatial location of the vanished stimulus. (C) Distractor task. Same as B, except the distractor is in the receptive field and the saccade target appears elsewhere. Adapted from .

Response of a neuron to a distractor flashed in its receptive field. Each panel shows a raster, spike density histogram and stimulus traces for fixation point, saccade target and distractor, and horizontal (Eh) and vertical (Ev) eye position. Shaded areas in the raster show stimulus, delay and distractor-activity periods used for quantitative analyses. (A) Response in the delayed saccade task synchronized on the stimulus appearance. (B) Same activity synchronized on the saccade onset. (C) Response of the same neuron to the stimulus flashed in the receptive field during the delay period of a saccade made outside the receptive field. (D) Response of the same neuron during the delay period of a saccade made to the receptive field. Adapted from .

Effect of saccade planning plotted across the sample. Each symbol represents a single cell, with the response to the distractor when the monkey plans a saccade away from the RF, plotted on the abscissa against the response to the distractor when the monkey plans a saccade into the RF, plotted on the ordinate. The response to stimulus appearance when the monkey makes a saccade away from the stimulus is significantly greater across the population of neurons than the response to the same stimulus when the monkey plans a saccade to the receptive field (p = 0.001, Wilcoxon paired signed-rank test). The dashed black line is the unity line. Figure reproduced with permission from .

Psychophysical attention task. (A) The monkeys began the trial by fixating a small spot (FP). After a short delay a second spot (the target) appeared for 100 ms at one of four possible positions equidistant from the fovea and evenly distributed throughout the four visual quadrants. The exact target locations varied from day to day, to prevent long-term perceptual learning. This target specified the goal for the memory-guided saccade that the monkey would have to make unless the probe told it otherwise. At some time after the target disappeared, a Landolt ring (the probe) and three complete rings of identical luminance to the probe flashed for one video frame (~17 ms) at the four possible saccade target positions. Five hundred milliseconds after the probe the fixation point disappeared, and the animals had to indicate the orientation of the Landolt ring by either maintaining fixation for 1000 ms (when the gap was on the right —a NOGO trial) or making a saccade to the goal and remaining there for 1000 ms (when the gap was on the left — a GO trial). The Landolt ring could appear at any of the four positions. The luminance of the rings varied from trial to trial, changing the contrast between the probe and the background. (B) In half of the trials a task-irrelevant distractor, identical to the target, was flashed 500 ms after the target either at or opposite the saccade goal. Reproduced with permission from .

Effect of saccade planning on perceptual threshold. (A) Psychometric functions from Monkey I from trials with a target-probe SOA of 1300 ms. The solid squares are from trials in which the probe was at the location of the target, the hollow circles are from trials in which the probe was not at the saccade goal. The data are pooled results from 22 sessions (approximately 800 trials per point). The performance from the two conditions was significantly different on the slopes of the functions (p<0.01, Chi-squared test at each contrast). The solid lines were fitted to the data with a Weibull function, weighted by the number of trials at each point, using the maximum likelihood method programmed in Matlab. (B) Normalized contrast thresholds for the three SOAs from the two monkeys when the probe was at the location of the saccade goal (solid triangles). Data for each delay were normalized by the performance at that delay when the probe was not at the saccade goal (illustrated by the dashed line). Points significantly beneath the dashed line show attentional enhancement, and all points were significant when tested with paired t-test comparing the pre-normalized performance when the probe was at the saccade goal with the prenormalized performance when the probe was away from the saccade goal. No distractor appeared in any of these trials. Reproduced with permission from .

Effect of the distractor on perceptual threshold. Data for each delay were normalized by the performance at that delay when the probe was not placed at the saccade goal in trials without a distractor (the same normalizing factor from ). In the trials shown here the distractor appeared opposite the saccade goal. Normalized contrast threshold was plotted against stimulus onset asynchrony (SOA) for trials in which the probe appeared at the saccade goal (blue symbols) or at the distractor site (red symbols). Performance for both animals was recorded at SOAs of 200, 700 and 1200 ms. Points significantly beneath the dashed line show attentional enhancement (*p<0.05, paired t-test on prenormalized data). Reproduced with permission from .

Neural activity and behavior in the attention task. (A) Raster diagram of response to the target appearing in the receptive field and to the distractor appearing outside of the receptive field (blue traces) and to the distractor appearing in the receptive field after the target had appeared outside of the receptive field (red traces). The thickness of the traces represents the standard error of the mean, and the solid blue and red bars show the time and duration of the target and distractor, respectively. (B) Spike density function calculated with a sigma of 10 ms from the same activity. These data were recorded while the monkey was performing the task on threshold. (C) Averaged normalized spike density functions from 18 cells from Monkey B. (D) Averaged normalized spike density functions from 23 cells from Monkey I. (E) and (F) Comparison of neural activity with behavior for each monkey. The top sections show the behavioral performance of the monkeys when the probe was placed at the saccade goal (blue data) or at the location of the distractor (red data in trials in which the target and distractor were in opposite locations. The triangles are data collected before the recording, and the circles are from data collected after recording the activity of LIP neurons in the same monkeys (red and blue traces in bottom section) The circle data were recorded at the crossing point in each monkey (455 ms for monkey B, 340 ms for monkey I) 500 ms later. Data were also collected from both animals at the crossing point recorded in the other animal. Statistical significance was confirmed with a paired t-test on the prenormalized data (*p<0.05). The black traces in the bottom section show the p-values from Wilcoxon paired signed-rank tests performed on the activity of all the neurons for a monkey over a 100-ms bin, measured every 5 ms. A low p-value (high on the axis) represents a significant difference in the activity from the two conditions. The gray column signifies when there is no statistical difference between the activity in both populations. The normalized spike density functions from have been superimposed to show the time course of activity in LIP following the onset of the distractor for the two monkeys. The thickness of the traces represents the standard error of the mean. (G–I) A comparison of the activity when the distractor, but not the saccade goal, was in the receptive field to the activity when the saccade goal, but not the distractor, was in the receptive field for one monkey. Solid circles represent cells with significant differences in response (t-test, p<0.05). (G) Mean activity 150–250 ms following the onset of the distractor for Monkey B. The responses were different across the population (p<0.001, Wilcoxon paired signed-rank test). (H) Mean activity during a 100-ms epoch centered at the crossing point for Monkey B (455 ms after the onset of the distractor). The responses were not different across the population (p>0.95). (I) Mean activity 600–700 ms following the onset of the distractor for Monkey B. The responses were different across the population (p<0.01).

Activity during error trials. (A) Comparison of activity in correct and incorrect trials. The mean activity of individual neurons in the 100 ms before the appearance of the probe in trials in which the target, but not the distractor, had appeared in the receptive field shown for incorrect (ordinate) and correct (abscissa) trials. Solid circles represent cells which had a significant difference by themselves (p<0.05 by t-test). Across the population there were significant response differences between correct and incorrect trials (p<0.001, Wilcoxon paired signed-rank test). (B) The mean activity in the 100 ms before the appearance of the probe in trials in which the distractor, but not the target, had appeared in the receptive field. Across the population there were significant response differences between correct and incorrect trials (p<0.001). Data in (A) and (B) are shown from the 30 neurons that had errors in both stimulus configurations. Adapted with permission from .

The response to the probe in the receptive field. (A) Spike density functions from the same neuron illustrated in . Data are from trials in which the monkey was instructed to plan a saccade into the receptive field and either the GO stimulus (black) or the NOGO stimulus (gray trace) appeared in the receptive field and from trials in which the saccade goal was opposite the receptive field and the GO probe appeared in the receptive field (dashed trace). The timing of the stimulus presentation is represented by the black bar starting at 0 ms. (B) The response to the NOGO stimulus plotted against the response to the GO stimulus in trials in which the monkey was instructed to plan a saccade to the receptive field. Data are from a 100-ms epoch starting at the onset of the probe. Solid circles are from cells in which the difference in activity was significant (p<0.05, t-test); hollow circles are from cells in which there was no significant difference. Across the population there was no difference in response to the two stimuli (p>0.15, Wilcoxon paired signed-rank test). (C) The response to the NOGO stimulus plotted against the response to the GO stimulus in trials in which the monkey was instructed to plan a saccade to the receptive field. Data are from a 150-ms epoch starting 100 ms after the onset of the probe. Across the population there was a significant difference in responses to the GO and NOGO stimuli (p<0.001). (D) The response to the NOGO stimulus plotted against the response to the GO stimulus in trials in which the monkey was instructed to plan a saccade away from the receptive field. Data are from a 150-ms epoch starting 100 ms after the onset of the probe. Across the population there was a significant difference in responses to the GO and NOGO stimuli (p<0.001). (E) The response to the complete ring plotted against the response to the GO stimulus in trials in which the monkey was instructed to plan and execute a saccade to the receptive field. Data are from a 150-ms epoch starting 100 ms after the onset of the probe. Across the population there was no difference in the responses to the GO and ring stimuli (p>0.6). (F) The response to the complete ring plotted against the response to the NOGO stimulus in trials in which the monkey was instructed to plan and then cancel a saccade to the receptive field. Data are from a 150-ms epoch starting 100 ms after the onset of the probe. Across the population there was a significant difference in the responses to the NOGO and circle stimuli (p<0.001). Adapted from .